Morshower co-starred with Enterprise guest actor James Avery in an unsold TV pilot entitled King's Pawn. Morshower's remaining TV credits during the 1990s include guest spots on Pensacola: Wings of Gold, with Michael Jace and Kristanna S. Loken, and The Crow: Stairway to Heaven, with John Pyper-Ferguson.

Morshower had a few feature film credits during the 1990s, as well. In 1992, Morshower played an ensign in the hit action film Under Siege, co-starring Bernie Casey and DS9 regular Colm Meaney. In 1994, Morshower was drafted into the Pauley Shore comedy film In the Army Now, co-starring Andy Dick and Lori Petty. Morshower was then seen in the action/thriller The River Wild, with William Lucking.

The new millennium brought Morshower numerous recurring roles. In 2000, he began appearing as Sheriff Brian Mobley on the hit CBS series CSI: Crime Scene Investigation. He was seen in six episodes throughout the show's first season (and one episode in the second), working alongside such Star Trek alumni as James Avery, Timothy Carhart, Gina Hecht, Gregg Henry, Gregory Itzin, Stephen Lee, Blake Lindsley, Mark Moses, Nicole Randall, Brenda Strong, and Tom Wright.

In 2004, Morshower guest-starred in two episodes of the popular spy series, Alias, created by J.J. Abrams. The following year, Morshower made two appearances on NBC's musical drama American Dreams, starring Ethan Dampf. His first American Dreams episode, "Home Again", also starred Jonathan Del Arco and Ellen Geer. That same year, Morshower was seen in two episodes of Charmed, both directed by James L. Conway, who previously worked with Morshower as the producer of 1979's The Bermuda Triangle. Morshower's most recent recurring role has been that of Chad Clarke on NBC's Friday Night Lights.

Morshower has portrayed Secret Service agent Aaron Pierce on 24 since the show's second episode in 2001. Morshower is the only actor other than series star Kiefer Sutherland to have appeared in all of the first seven seasons of the show (Morshower did not appear in the final season). In 2007, he and his various co-stars from this series – including Jude Ciccolella, Roger R. Cross, and Gregory Itzin (whom Morshower has worked with many times before) – were nominated with a Screen Actors Guild Award for Outstanding Performance by an Ensemble in a Drama Series.

In 2004, Morshower appeared on Crossing Jordan, the NBC medical drama which starred Miguel Ferrer. He then guest-starred on HBO's hit western series Deadwood, on which Jim Beaver, Brad Dourif, Paula Malcomson, and Leon Rippy were regulars and Keith Carradine, Zach Grenier, Clay Wilcox, and Keone Young had recurring roles. Morshower later appeared in an episode of Neal McDonough's short-lived NBC series Medical Investigation, along with Art Chudabala.

Morshower had a small role in the 2001 biographical movie Blonde, starring Kirstie Alley, Wallace Shawn, and Titus Welliver. In 2004, he appeared with Megan Gallagher, Leland Orser, and Tracy Scoggins in the drama Homeland Security. That same year he co-starred in Category 6: Day of Destruction with Brian Markinson. His most recent made-for-TV movie was 2005's Walker, Texas Ranger: Trial by Fire, along with Marshall Teague and Ned Vaughn.